Extracellular Electron Transfer across Bacterial Cell Membranes via a Cytocompatible Redox-Active Polymer

Multiheme cytochromes, located on the bacterial cell surface, function as long-distance (> 10 nm) electron conduits linking intracellular reactions to external surfaces. This extracellular electron transfer process, which allows microorganisms to gain energy by respiring solid redox-active minerals, also facilitates the wiring of cells to electrodes. While recent studies suggested that a chiral induced spin selectivity effect is linked to efficient electron transmission through biomolecules, this phenomenon has not been investigated in the extracellular electron conduits. Using magnetic conductive probe atomic force microscopy, Hall voltage measurements, and spin-dependent electrochemistry of the decaheme cytochromes MtrF and OmcA from the metal-reducing bacterium <i>Shewanella oneidensis</i> MR-1, we show that electron transport through these extracellular conduits is spin-selective. Our study has implications for understanding how spin-dependent interactions and magnetic fields may control electron transport across biotic-abiotic interfaces in both natural and biotechnological systems.

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Acceleration of Extracellular Electron Transfer by Alternative Redox-Active Molecules to Riboflavin for Outer-Membrane Cytochrome c of Shewanella oneidensis MR-1

The Journal of Physical Chemistry C ◽

10.1021/acs.jpcc.6b00349 ◽

2016 ◽

Vol 120 (29) ◽

pp. 16168-16173 ◽

Cited By ~ 19

Author(s):

Yoshihide Tokunou ◽

Kazuhito Hashimoto ◽

Akihiro Okamoto

Keyword(s):

Electron Transfer ◽

Cytochrome C ◽

Outer Membrane ◽

Shewanella Oneidensis ◽

Extracellular Electron Transfer ◽

Redox Active

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Molecular design of cytocompatible amphiphilic redox-active polymers for efficient extracellular electron transfer

Bioelectrochemistry ◽

10.1016/j.bioelechem.2016.11.001 ◽

2017 ◽

Vol 114 ◽

pp. 8-12 ◽

Cited By ~ 15

Author(s):

Masahiro Kaneko ◽

Masahito Ishikawa ◽

Kazuhito Hashimoto ◽

Shuji Nakanishi

Keyword(s):

Electron Transfer ◽

Molecular Design ◽

Extracellular Electron Transfer ◽

Redox Active

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Geothrix fermentans Secretes Two Different Redox-Active Compounds To Utilize Electron Acceptors across a Wide Range of Redox Potentials

Applied and Environmental Microbiology ◽

10.1128/aem.01460-12 ◽

2012 ◽

Vol 78 (19) ◽

pp. 6987-6995 ◽

Cited By ~ 44

Author(s):

Misha G. Mehta-Kolte ◽

Daniel R. Bond

Keyword(s):

Electron Transfer ◽

Redox Potential ◽

Electron Acceptor ◽

Extracellular Electron Transfer ◽

Redox Potentials ◽

Active Compounds ◽

Content Type ◽

Electron Shuttles ◽

Redox Active ◽

Geothrix Fermentans

ABSTRACTThe current understanding of dissimilatory metal reduction is based primarily on isolates from the proteobacterial generaGeobacterandShewanella. However, environments undergoing active Fe(III) reduction often harbor less-well-studied phyla that are equally abundant. In this work, electrochemical techniques were used to analyze respiratory electron transfer by the only known Fe(III)-reducing representative of theAcidobacteria,Geothrix fermentans. In contrast to previously characterized metal-reducing bacteria, which typically reach maximal rates of respiration at electron acceptor potentials of 0 V versus standard hydrogen electrode (SHE),G. fermentansrequired potentials as high as 0.55 V to respire at its maximum rate. In addition,G. fermentanssecreted two different soluble redox-active electron shuttles with separate redox potentials (−0.2 V and 0.3 V). The compound with the lower midpoint potential, responsible for 20 to 30% of electron transfer activity, was riboflavin. The behavior of the higher-potential compound was consistent with hydrophilic UV-fluorescent molecules previously found inG. fermentanssupernatants. Both electron shuttles were also produced when cultures were grown with Fe(III), but not when fumarate was the electron acceptor. This study reveals thatGeothrixis able to take advantage of higher-redox-potential environments, demonstrates that secretion of flavin-based shuttles is not confined toShewanella, and points to the existence of high-potential-redox-active compounds involved in extracellular electron transfer. Based on differences between the respiratory strategies ofGeothrixandGeobacter, these two groups of bacteria could exist in distinctive environmental niches defined by redox potential.

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Bacterial microcompartments linked to the flavin-based extracellular electron transfer drives anaerobic ethanolamine utilization in Listeria monocytogenes

10.1101/2020.10.27.358424 ◽

2020 ◽

Author(s):

Zhe Zeng ◽

Sjef Boeren ◽

Varaang Bhandula ◽

Samuel H. Light ◽

Eddy J. Smid ◽

...

Keyword(s):

Electron Transfer ◽

Listeria Monocytogenes ◽

Electron Acceptor ◽

Cell Membranes ◽

Anaerobic Growth ◽

Extracellular Electron Transfer ◽

Severe Illness ◽

Redox Imbalance ◽

Bacterial Microcompartments

AbstractEthanolamine (EA) is a valuable microbial carbon and nitrogen source derived from phospholipids present in cell membranes. EA catabolism is suggested to occur in so-called bacterial microcompartments (BMCs) and activation of EA utilization (eut) genes is linked to bacterial pathogenesis. Despite reports showing that activation of eut in Listeria monocytogenes is regulated by a vitamin B12-binding riboswitch and that upregulation of eut genes occurs in mice, it remains unknown whether EA catabolism is BMC dependent. Here, we provide evidence for BMC-dependent anaerobic EA utilization via metabolic analysis, proteomics and electron microscopy. First, we show B12-induced activation of the eut operon in L. monocytogenes coupled to uptake and utilization of EA thereby enabling growth. Next, we demonstrate BMC formation in conjunction to EA catabolism with the production of acetate and ethanol in a molar ratio of 2:1. Flux via the ATP generating acetate branch causes an apparent redox imbalance due to reduced regeneration of NAD+ in the ethanol branch resulting in a surplus of NADH. We hypothesize that the redox imbalance is compensated by linking eut BMC to anaerobic flavin-based extracellular electron transfer (EET). Using L. monocytogenes wild type, a BMC mutant and a EET mutant, we demonstrate an interaction between BMC and EET and provide evidence for a role of Fe3+ as an electron acceptor. Taken together, our results suggest an important role of anaerobic BMC-dependent EA catabolism in the physiology of L. monocytogenes, with a crucial role for the flavin-based EET system in redox balancing.IMPORTANCEListeria monocytogenes is a food-borne pathogen causing severe illness and, as such, it is crucial to understand the molecular mechanisms contributing to pathogenicity. One carbon source that allows L. monocytogenes to grow in humans is ethanolamine (EA), which is derived from phospholipids present in eukaryotic cell membranes. It is hypothesized that EA utilization occurs in bacterial microcompartments (BMCs), self-assembling subcellular proteinaceous structures and analogs of eukaryotic organelles. Here, we demonstrate that BMC-driven utilization of EA in L. monocytogenes results in increased energy production essential for anaerobic growth. However, exploiting BMCs and the encapsulated metabolic pathways also requires balancing of oxidative and reductive pathways. We now provide evidence that L. monocytogenes copes with this by linking BMC activity to flavin-based extracellular electron transfer (EET) using iron as an electron acceptor. Our results shed new light on an important molecular mechanism that enables L. monocytogenes to grow using host-derived phospholipid degradation products.

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Microbial electroactive biofilms dominated by Geoalkalibacter spp. from a highly saline–alkaline environment

npj Biofilms and Microbiomes ◽

10.1038/s41522-020-00147-7 ◽

2020 ◽

Vol 6 (1) ◽

Author(s):

Sukrampal Yadav ◽

Sunil A. Patil

Keyword(s):

Electron Transfer ◽

Amplicon Sequencing ◽

Extracellular Electron Transfer ◽

Microbial Electrochemistry ◽

16S Rrna Amplicon Sequencing ◽

Redox Active ◽

Lonar Lake ◽

Current Densities ◽

The Mean

Abstract Understanding of the extreme microorganisms that possess extracellular electron transfer (EET) capabilities is pivotal to advance electromicrobiology discipline and to develop niche-specific microbial electrochemistry-driven biotechnologies. Here, we report on the microbial electroactive biofilms (EABs) possessing the outward EET capabilities from a haloalkaline environment of the Lonar lake. We used the electrochemical cultivation approach to enrich haloalkaliphilic EABs under 9.5 pH and 20 g/L salinity conditions. The electrodes controlled at 0.2 V vs. Ag/AgCl yielded the best-performing biofilms in terms of maximum bioelectrocatalytic current densities of 548 ± 23 and 437 ± 17 µA/cm2 with acetate and lactate substrates, respectively. Electrochemical characterization of biofilms revealed the presence of two putative redox-active moieties with the mean formal potentials of 0.183 and 0.333 V vs. Ag/AgCl, which represent the highest values reported to date for the EABs. 16S-rRNA amplicon sequencing of EABs revealed the dominance of unknown Geoalkalibacter sp. at ~80% abundance. Further investigations on the haloalkaliphilic EABs possessing EET components with high formal potentials might offer interesting research prospects in electromicrobiology.

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Spin-Dependent Electron Transport through Bacterial Cell Surface Multiheme Electron Conduits

10.26434/chemrxiv.9748046 ◽

2019 ◽

Author(s):

Suryakant Mishra ◽

Sahand Pirbadian ◽

Amit Kumar Mondal ◽

Moh El-Naggar ◽

Ron Naaman

Keyword(s):

Electron Transport ◽

Cell Surface ◽

Bacterial Cell ◽

Shewanella Oneidensis ◽

Extracellular Electron Transfer ◽

Long Distance ◽

Force Microscopy ◽

Bacterial Cell Surface ◽

Redox Active ◽

Gain Energy

Multiheme cytochromes, located on the bacterial cell surface, function as long-distance (> 10 nm) electron conduits linking intracellular reactions to external surfaces. This extracellular electron transfer process, which allows microorganisms to gain energy by respiring solid redox-active minerals, also facilitates the wiring of cells to electrodes. While recent studies suggested that a chiral induced spin selectivity effect is linked to efficient electron transmission through biomolecules, this phenomenon has not been investigated in the extracellular electron conduits. Using magnetic conductive probe atomic force microscopy, Hall voltage measurements, and spin-dependent electrochemistry of the decaheme cytochromes MtrF and OmcA from the metal-reducing bacterium <i>Shewanella oneidensis</i> MR-1, we show that electron transport through these extracellular conduits is spin-selective. Our study has implications for understanding how spin-dependent interactions and magnetic fields may control electron transport across biotic-abiotic interfaces in both natural and biotechnological systems.

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Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms

10.1101/2019.12.12.872085 ◽

2019 ◽

Cited By ~ 1

Author(s):

Scott H. Saunders ◽

Edmund C.M. Tse ◽

Matthew D. Yates ◽

Fernanda Jiménez Otero ◽

Scott A. Trammell ◽

...

Keyword(s):

Pseudomonas Aeruginosa ◽

Electron Transfer ◽

Redox Reactions ◽

Extracellular Dna ◽

Extracellular Electron Transfer ◽

Bacterial Biofilms ◽

Active Metabolites ◽

Electron Shuttles ◽

Redox Active

SUMMARYExtracellular electron transfer (EET), the process whereby cells access electron acceptors or donors that reside many cell lengths away, enables metabolic activity by microorganisms, particularly under oxidant-limited conditions that occur in multicellular bacterial biofilms. Although different mechanisms underpin this process in select organisms, a widespread strategy involves extracellular electron shuttles, redox-active metabolites that are secreted and recycled by diverse bacteria. How these shuttles catalyze electron transfer within biofilms without being lost to the environment has been a long-standing question. Here, we show that phenazine electron shuttles mediate efficient EET through interactions with extracellular DNA (eDNA) in Pseudomonas aeruginosa biofilms, which are important in nature and disease. Retention of pyocyanin (PYO) and phenazine carboxamide in the biofilm matrix is facilitated by binding to eDNA. In vitro, different phenazines can exchange electrons in the presence or absence of DNA and phenazines can participate directly in redox reactions through DNA; the biofilm eDNA can also support rapid electron transfer between redox active intercalators. Electrochemical measurements of biofilms indicate that retained PYO supports an efficient redox cycle with rapid EET and slow loss from the biofilm. Together, these results establish that eDNA facilitates phenazine metabolic processes in P. aeruginosa biofilms, suggesting a model for how extracellular electron shuttles achieve retention and efficient EET in biofilms.

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Improper Localization of the OmcS Cytochrome May Explain the Inability of thexapD-Deficient Mutant ofGeobacter sulfurreducensto Reduce Fe(III) Oxide

10.1101/114900 ◽

2017 ◽

Cited By ~ 8

Author(s):

Kelly A. Flanagan ◽

Ching Leang ◽

Joy E. Ward ◽

Derek R. Lovley

Keyword(s):

Electron Transfer ◽

Electron Transport ◽

Type Strain ◽

Wild Type Strain ◽

Geobacter Sulfurreducens ◽

Extracellular Electron Transfer ◽

Outer Cell ◽

Wild Type ◽

Redox Active ◽

In The Wild

AbstractExtracellular electron transfer through a redox-active exopolysaccharide matrix has been proposed as a strategy for extracellular electron transfer to Fe(III) oxide byGeobacter sulfurreducens,based on the phenotype of axapD-deficient strain. Central to this model was the assertion that thexapD-deficient strain produced pili decorated with the multi-hemec-type cytochrome OmcS in manner similar to the wild-type strain. Further examination of thexapD-deficient strain with immunogold labeling of OmcS and transmission electron microscopy revealed that OmcS was associated with the outer cell surface rather than pili. PilA, the pilus monomer, could not be detected in thexapD-deficient strain under conditions in which it was readily detected in the wild-type strain. Multiple lines of evidence in previous studies have suggested that long-range electron transport to Fe(III) oxides proceeds through electrically conductive pili and that OmcS associated with the pili is necessary for electron transfer from the pili to Fe(III) oxides. Therefore, an alternative explanation for the Fe(III) oxide reduction phenotype of thexapD-deficientstrain is that the pili-OmcS route for extracellular electron transport to Fe(III) oxide has been disrupted in thexapD-deficient strain.

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